Reduced representation genome sequencing suggests low diversity on the sex chromosomes of tonkean macaque monkeys

Mol Biol Evol. 2014 Sep;31(9):2425-40. doi: 10.1093/molbev/msu197. Epub 2014 Jul 1.

Abstract

In species with separate sexes, social systems can differ in the relative variances of male versus female reproductive success. Papionin monkeys (macaques, mangabeys, mandrills, drills, baboons, and geladas) exhibit hallmarks of a high variance in male reproductive success, including a female-biased adult sex ratio and prominent sexual dimorphism. To explore the potential genomic consequences of such sex differences, we used a reduced representation genome sequencing approach to quantifying polymorphism at sites on autosomes and sex chromosomes of the tonkean macaque (Macaca tonkeana), a species endemic to the Indonesian island of Sulawesi. The ratio of nucleotide diversity of the X chromosome to that of the autosomes was less than the value (0.75) expected with a 1:1 sex ratio and no sex differences in the variance in reproductive success. However, the significance of this difference was dependent on which outgroup was used to standardize diversity levels. Using a new model that includes the effects of varying population size, sex differences in mutation rate between the autosomes and X chromosome, and GC-biased gene conversion (gBGC) or selection on GC content, we found that the maximum-likelihood estimate of the ratio of effective population size of the X chromosome to that of the autosomes was 0.68, which did not differ significantly from 0.75. We also found evidence for 1) a higher level of purifying selection on genic than nongenic regions, 2) gBGC or natural selection favoring increased GC content, 3) a dynamic demography characterized by population growth and contraction, 4) a higher mutation rate in males than females, and 5) a very low polymorphism level on the Y chromosome. These findings shed light on the population genomic consequences of sex differences in the variance in reproductive success, which appear to be modest in the tonkean macaque; they also suggest the occurrence of hitchhiking on the Y chromosome.

Keywords: GC-biased gene conversion; X chromosome; Y chromosome; demography; male driven evolution; molecular polymorphism.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Base Composition
  • Chromosomes, Mammalian / genetics*
  • Evolution, Molecular
  • Female
  • Genetic Variation
  • Genome
  • Indonesia
  • Likelihood Functions
  • Macaca / classification
  • Macaca / genetics*
  • Male
  • Mutation Rate
  • Polymorphism, Genetic
  • Population Density
  • Reproduction
  • Selection, Genetic
  • Sequence Analysis, DNA / methods*
  • Sex Chromosomes / genetics*
  • Sex Ratio